A fresh look at microplastics and other particles in the tropical coastal ecosystems of Tamandaré, Brazil
Introduction
Plankton organisms, biogenic particles, inorganic mineral particles, and microplastics are the four main components of particulate organic matter in aquatic ecosystems (Fleming et al., 2019; Bowers and Binding, 2006; Nakajima et al., 2010; Vroom et al., 2017; Lins Silva et al., 2019). However, there are no published studies available yet, which consider these four components in a synoptic way and compare their distribution patterns.
Suspended particles are key elements in marine ecosystems, mainly because of their role in fueling food webs and biogeochemical cycles, such as the biological “carbon pump” (Schumann and Rentsch, 1998; Schwamborn et al., 2002, 2006; Checkley et al., 2008). Recent studies showed that non-organismic particles (particles that do not constitute a single living organism, e.g., detritus, aggregates, sand grains and microplastics) constitute a significant portion of common plankton samples, leading to an overestimation of plankton biomass in the oceans (Nakajima et al., 2010; Ohman et al., 2012; Lins Silva et al., 2019). In estuarine and coastal waters, ignoring the huge contribution of particles may lead to a severe underestimation of seston biomass by traditional wet weight-based methods (Lins Silva et al., 2019). Coastal tropical environments, such as mangroves and coral reefs, receive many terrigenous materials. Also, nearshore coastal ecosystems may show high concentrations of anthropogenic particles, such as microplastics (Chong et al., 2001; Barnes et al., 2009).
Zooplankton, biogenic particles and microplastics are traditionally studied by means of sampling with fine-meshed nets and manual counts under a microscope (Blanchot et al., 1989; Neumann-Leitão et al., 1998). Since manual sorting, identification, and quantification of particles and plankton are a time-consuming task, image analysis has become a popular tool in the last ~30 years. Benchtop imaging devices, such as the ZooScan (Grosjean et al., 2004), provide good quality images, with almost perfect focus. Fourier-Transformed Infrared Spectroscopy (FTIR) can be used to identify polymers and to investigate the chemical composition and weathering of microplastics (Dutra et al., 1995; Munajad et al., 2018). Extensive protocols for the preparation of microplastic samples have been developed, including slow and complex dehydration procedures, to allow a reliable interpretation of FTIR spectra (Dutra et al., 1995; Pinho and Macedo 2005). Different sample preparation techniques have been applied, since the methods to separate polymers from other components depend on the diversity of particle types (Dutra et al., 1995; Pinho and Macedo 2005; Munajad et al., 2018). Few studies have used FTIR to analyze microplastics taken from plankton net samples (Di Mauro et al., 2017; Cincinelli et al., 2017), and none have yet combined ZooScan and FTIR to distinguish plankton organisms, biogenic particles and microplastics.
Although there are few studies that estimated the chemical composition and characterization of these particles (McCave et al., 2001; Cincinelli et al., 2017), there are no studies about the origin (anthropogenic or natural) and type (chemical markers) of suspended particles in tropical marine environments.
In spite of the vast recent literature on this subject, there is no practical approach available for the assessment of contamination with microplastics, that explicitly considers the relative contribution of these pollutants, with regard to the available food (suspended particles and plankton) in the water column. This is probably due to the fact that most studies on microplastics destroy and digest biogenic particles and plankton in the samples with acids or enzymes, previous to counting microplastics. The few studies that actually consider microplastics/zooplankton ratios (Cole et al., 2013; Botterell et al., 2019), but do not consider non-organismic biogenic particles, such as plant detritus (Schwamborn et al., 2006), carcases (Silva et al., 2020), and marine aggregates (Kvale et al., 2020).
In the present study, we suggest a new approach and a new index (RMC) to analyze contamination with microplastics. Furthermore, we used this new approach to test the hypothesis that particle type, concentration and volume (in absolute and relative units), differ between ecosystems (mangrove estuary, coral reef-lined bay and continental shelf), thus helping to reveal sources and sinks of biogenic and anthropogenic particles. Also, we aim at discerning the ecosystems that are most impacted by different types of microplastics.
Section snippets
Study area
The sampled areas range from highly turbid, “brown” estuarine waters, lined by mangroves, to clear “green” waters at nearby coral reefs, and oligotrophic “blue“ waters at mid-shelf. The Rio Formoso Estuary (8° 39' - 8° 42′S and 35°10' - 35° 05′W) extends over 12 km and along its route, it receives wastes from domestic sewage and sugar cane industry (Fidem, 1987; CPRH, 1999). The Rio Formoso Estuary is located ~4 Km North of the Tamandaré Bay. The estuarine channels are entirely bordered by
Hydrographic features
The three study areas (Rio Formoso Estuary, Tamandaré Bay and Continental Shelf) showed characteristic hydrographic features (Fig. 2). Significantly (p < 0.0001) lower transparency was found in the Estuary (Secchi depth range: 1.2–3.5 m; mean: 1.8 m) than in the Bay (1.0–5.5 m; mean: 3.1 m) and on the Shelf (1.0–19.0 m; mean: 5.3 m). Euhaline conditions were found in the Bay (salinity range: 35.0–36.5; mean: 35.9) and on the Shelf (33.8–37.4; mean: 36.3). Conversely, mesohaline to euhaline
Discussion
This study provides new insights into the distribution of microplastics and other suspended particles in tropical estuarine and marine environments, combining two different optical methods (ZooScan and FTIR). Through the use of a new approach and new indices, we quantified the contributions of different types of particles in the meso (>299 μm) size range, natural or not, as ecosystem components. This approach allows novel interpretations of the composition of robust, large-sized seston in the
Conclusions
This study provided new insights into the distribution of microplastics within the available food spectrum in tropical coastal areas. The composition of biogenic particles followed the expected pattern, with more plant matter (mangrove detritus) in the mangrove-lined estuary. Surprisingly, the impact of microplastics was more severe in offshore waters than at the river mouths (the sources of anthropogenic particles). In short, Bay and nearshore shelf waters were the most severely impacted areas
CRediT authorship contribution statement
Nathália Lins-Silva: Conceptualization, Formal analysis, Funding acquisition. Catarina R. Marcolin: Conceptualization, Formal analysis, Funding acquisition. Felipe Kessler: Conceptualization, Formal analysis, Funding acquisition. Ralf Schwamborn: Conceptualization, Formal analysis, Funding acquisition.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
The authors thank the Brazilian National Research Council (CNPq) for the productivity fellowship granted to the last author. Fieldwork was funded by the ESPLAN project (CNPq grant no. 471038/2012-1) and by INCTAmbTropic (CNPq/CAPES/FAPESB). We also thank the Long Term Ecological Research Program PELD-TAMS (MCTI/CNPq), and to the Instituto Recifes Costeiros (IRCOS, supported by ICMBio, SOS Mata Atlântica and Toyota do Brasil Foundations), for logistical support with sampling. This paper was
References (88)
- et al.
Bioavailability and effects of microplastics on marine zooplankton: a review
Environ. Pollut.
(2019) - et al.
The optical properties of mineral suspended articles: a review and synthesis
Estuarine, Coast. Shelf Sci.
(2006) - et al.
Microplastic in the surface waters of the Ross Sea (Antarctica) Occurrence, distribution and characterization by FTIR
J. Chemos.
(2017) - et al.
Microplastics as contaminants in the marine environment: a review
Mar. Pollut. Bull.
(2011) The pollution of the marine environment by plastic debris: a review
Mar. Pollut. Bull.
(2002)- et al.
Abundant plankton-sized microplastic particles in shelf waters of the northern Gulf of Mexico
Environ. Pollut.
(2017) - et al.
Using image analysis to assess the contributions of plankton and particles to tropical coastal ecosystems
Estuar. Coast Shelf Sci.
(2019) - et al.
Distribution, composition and flux of particulate nnnnmaterial over the European margin at 47° – 50° N. Deep Sea Research
Part II: Top. Stud. Oceanogr.
(2001) - et al.
A comparison of plastic and plankton in the north pacific center gyre
Mar. Pollut. Bull.
(2001) - et al.
Non-predatory mortality of planktonic copepods in a reef area influenced by estuarine plume
Mar. Environ. Res.
(2020)
Ingestion of microplastics by natural zooplankton groups in the northern South China Sea
Mar. Pollut. Bull.
A critical view on microplastic quantification in aquatic organisms
Environ. Res.
Assessing biases in computing size spectra of automatically classified zooplankton from imaging systems: a case study with the ZooScan integrated system
Methods Oceanogr. J.
A new method for non‐parametric multivariate analysis of variance
Austral Ecol.
Permutational Multivariate Analysis of Variance (PERMANOVA)
Plastics in the environment
Skeletal variability of the coral Favia gravida (Verrill, 1868) from Brazil
Biota Neotropica
Análise quali-quantitativa do lixo deixado na Baía de Tamandaré-PE-Brasil, por excursionistas
Plastics and microplastics in the oceans: from emerging pollutants to emerged threat
Mar. Environ. Res.
Accumulation and fragmentation of plastic debris in global environments
Philos. Trans. R. Soc.
Size composition of particulate organic matter in the lagoon of Tikehau atoll (Tuamotu archipelago)
Mar. Biol.
Ingested microscopic plastic translocates to the circulatory system of the mussel, Mytilus edulis (L.)
Environ. Sci. Technol.
Morfologia da plataforma continental interna adjacente ao município de Tamandaré, Sul de Pernambuco – Brasil
Rev. Bras. Geofís.
Assessing plankton and other particles in situ with the SOLOPC
Limnol. Oceanogr.
Contribution of mangrove detritus to juvenile prawn nutrition: a dual stable isotope study in a Malaysian mangrove forest
Mar. Biol.
Microplastic ingestion by zooplankton
Environ. Sci. Technol. Davis.
The impact of polystyrene microplastics on feeding, function and fecundity in the marine copepod Calanus helgolandicus
Environ. Sci. Technol.
Neustonic microplastic and zooplankton in the north western Mediterranean Sea
Mar. Pollut. Bull.
Plano de Gestão, Zoneamento Ecológico Econômico Costeiro – ZEEC – APA de Guadalupe Litoral Sul de Pernambuco
Statistical comparisons of classifiers over multiple data sets
J. Mach. Learn. Res.
Ingestion of microplastics by zooplankton in the northeast pacific ocean
Arch. Environ. Contam. Toxicol.
Importância da Preparação de Amostras em Espectroscopia no Infravermelho com Transformada de Fourier (FTIR) na Investigação de Constituintes em Materiais Compostos
Polímeros - Cienc. Tecnol.
Kelp detritus provides high-quality food for sea urchin larvae
Limnol. Oceanogr.
Interações entre a pesca artesanal e o turismo em Tamandaré
Proteção das áreas estuarinas. Recife. (Séries Desenvolvimento Urbano e Meio Ambiente)
Influence of mangrove detritus in an estuarine ecosystem
Bull. Mar. Sci.
Variação nictemeral do fitoplâncton e elementos nutrientes no canal de Santa Cruz, Itamaracá-PE, Brasil
Trab. Oceanogr. Univ. Fed. Pernamb.
Coastal and Estuarine Management
Global Distribution, Composition and Abundance of Marine Litter
Sustentabilidade Dos Oceanos, Blucher
Digital zooplankton image analysis using the ZooScan integrated system
J. Plankton Res.
Fitoplâncton do ecossistema estuarino do Rio Ariquindá (Tamandaré, Pernambuco, Brasil): variáveis ambientais, biomassa e produtividade primária
Atlântica, Rio Grande
Enumeration, measurement, and identification of net zooplankton samples using the ZOOSCAN digital imaging system
ICES J. Mar. Sci.
Nonparametric Statistical Methods
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